Published on Web 08/20/2005
Axial Ligand Substituted Nonheme FeIVdO Complexes: Observation of Near-UV LMCT Bands and FedO Raman Vibrations Chivukula V. Sastri,† Mi Joo Park,† Takehiro Ohta,‡ Timothy A. Jackson,| Audria Stubna,§ Mi Sook Seo,† Jimin Lee,† Jinheung Kim,† Teizo Kitagawa,*,‡ Eckard Mu¨nck,*,§ Lawrence Que, Jr.,*,| and Wonwoo Nam*,† Department of Chemistry and Center for Biomimetic Systems, Ewha Womans UniVersity, Seoul 120-750, Korea, Okazaki Institute for IntegratiVe Bioscience, National Institutes of Natural Sciences, Okazaki, Japan, Department of Chemistry, Carnegie Mellon UniVersity, Pittsburgh, PennsylVania 15213, and Department of Chemistry and Center for Metals in Biocatalysis, UniVersity of Minnesota, Minneapolis, Minnesota 55455 Received June 20, 2005; E-mail:
[email protected];
[email protected] High-valent oxoiron(IV) intermediates have been implicated as the active oxidizing species in metabolically important oxidative transformations performed by mononuclear nonheme iron enzymes.1 Very recently, such oxoiron(IV) species were directly observed in enzymatic and biomimetic reactions.2,3 For example, an intermediate with a high-spin oxoiron(IV) unit was identified in the catalytic cycle of Escherichia coli taurine:RKG dioxygenase (TauD).2 In biomimetic studies, mononuclear nonheme oxoiron(IV) complexes bearing tetradentate N4 and pentadentate N5 ligands were synthesized and characterized with various spectroscopic techniques, and the reactivities of these complexes were investigated in a number of oxidation reactions.3 In heme iron enzymes, proximal ligands, such as cysteine (cytochrome P450), histidine (peroxidase), and tyrosine (catalase), are believed to play crucial roles in generating and tuning reactivities of oxoiron(IV) porphyrin π-cation radicals, the so-called Compound I (Cpd I) state.4 Indeed, it has been well demonstrated in iron porphyrin models that the reactivity and spectroscopic properties of Cpd I are markedly influenced by the axial ligands trans to the iron-oxo moiety.5,6 We are, therefore, exploring the axial ligand effect on the chemical properties of nonheme oxoiron(IV) complexes. In this communication, we report that axial ligand substitution of a mononuclear nonheme oxoiron(IV) complex, [FeIV(O)(TMC)(NCCH3)]2+ (1) (TMC ) 1,4,8,11-tetramethyl-1,4,8,11-tetraazacyclotetradecane),3a leads to the formation of new FeIVdO species with relatively intense electronic absorption features in the near-UV region. The presence of these near-UV features permits the first observation of FedO vibrations using resonance Raman spectroscopy. We also report that the oxidizing power of the oxoiron(IV) species is significantly affected by the identity of the axial ligand. The reaction of [FeII(TMC)(X)(CF3SO3)] (2-NCS and 2-N3 for X ) NCS- and N3-, respectively)7 with 1.2 equiv of PhIO in CH3CN at 25 °C affords 1-NCS and 1-N3, respectively, that exhibit the electronic spectra shown in Figure 1. To establish the elemental composition of 1-NCS and 1-N3, electrospray ionization mass spectrometry (ESI MS) experiments were performed. The ESI mass spectra of 1-NCS and 1-N3 exhibit prominent ion peaks at m/z ) 386.1 and 370.1, respectively (Supporting Information, Figure S3), which both upshift accordingly upon introduction of 18O when PhI18O is used instead of PhI16O to generate the intermediates. These data are consistent with the formulation of 1-NCS and 1-N3 as [FeIV(O)(TMC)(NCS)]+ and [FeIV(O)(TMC)(N3)]+, respectively, where the oxo ligands are derived from PhIO. † Ewha Womans University. ‡ National Institutes of Natural | University of Minnesota. § Carnegie Mellon University.
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Figure 1. UV-vis spectra of [FeIV(O)(TMC)(NCS)]+ (red), [FeIV(O)(TMC)(N3)]+ (blue), and [Fe IV(O)(TMC)(NCCH3)]2+ (black). Inset shows the expanded near-IR absorptions. Table 1. Properties of FeIV(O)(TMC)(X) Complexes X)
NCCH3
N3-
NCS-
λmax (nm)
282 (10000)b 820 (400)a
ν(FedO) (cm-1) δ (mm/s) EQ (mm/s) kox(PPh3) (M-1 s-1)
834a 0.17a 1.23a 6.4
407 (3600)b 850 (130)b 1050 (110)b 812 0.17 0.70 0.61
387 (3500)b 850 (200)b 1010 (170)b 820 0.18 0.55 0.22
a From ref 3a. b The corresponding (M-1 cm-1) values are given in parentheses.
To probe the oxidation and spin states of the iron centers in 1-NCS and 1-N3, zero-field Mo¨ssbauer spectra were obtained (Table 1). 1-NCS and 1-N3 have isomer shifts (δ) of 0.18 and 0.17 mm/s, respectively, which are virtually identical to that of parent complex 1 (Table 1). As the δ value is sensitive to the oxidation and spin state of iron centers and given the results of our ESI MS studies, we conclude that 1-NCS and 1-N3 contain S ) 1 FeIVdO units. It is interesting, however, that both 1-NCS and 1-N3 exhibit smaller quadrupole splitting parameters (∆EQ) than 1 (Table 1), indicating perturbation of the ground-state electronic structure of the FeIVdO unit by the axial ligation of NCS- and N3-. Further evidence for electronic perturbation imposed by the presence of these anionic ligands is provided by comparing the electronic absorption spectra of 1-NCS and 1-N3 with that of 1 (Figure 1; Table 1). Relative to 1, the near-IR absorption features of 1-NCS and 1-N3 are red-shifted and significantly less intense (Figure 1; Table 1), similar to what was observed when the NCCH3 ligand of 1 was replaced with trifluoroacetate.8 As the near-IR features of S ) 1 FeIVdO complexes are known to arise from FeIV d f d transitions,9 the red-shifting of the near-IR features upon 10.1021/ja0540573 CCC: $30.25 © 2005 American Chemical Society
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Figure 2. Resonance Raman spectra of (a) [Fe(16O)(TMC)(NCS)]+ (black) and (b) [Fe(18O)(TMC)(NCS)]+ (red) in CH3CN obtained at -20 °C with 406.7 nm excitation. The peaks marked with s are from solvent.
NCS- and N3- binding suggests that these anions impose a weaker ligand field than NCCH3. Perhaps most striking of the properties of 1-NCS and 1-N3 are the intense new bands at 387 and 407 nm, respectively (Figure 1; Table 1), which are not observed in the parent oxoiron(IV) complex 1.3a Resonance Raman (RR) experiments were performed to gain insight into the nature of these unique electronic transitions. The RR spectrum of 1-NCS exhibits a vibration at 820 cm-1 that shifts to 786 cm-1 upon introduction of 18O (Figure 2). This observed isotopic shift of -34 cm-1 with 18O-substitution is in good agreement with the calculated value (∆νcalcd ) -33 cm-1) for an Fe-O diatomic vibration. Thus, we assign this RR feature as the ν(FedO) mode of 1-NCS. The RR spectrum of 1-N3 displays a vibration at 812 cm-1 that shifts to 779 cm-1 upon introduction of 18O (Supporting Information, Figure S4), which we assign as the corresponding ν(FedO) mode of 1-N3. Importantly, these represent the first Raman observations of ν(FedO) vibrations for nonheme S ) 1 FeIVdO complexes. In contrast, the ν(FedO) frequency of 1 was observed at 834 cm-1 using Fourier transform infrared spectroscopy (Table 1).3a RR spectroscopy was used, however, to determine the ν(FedO) energy for the high-spin oxoiron(IV) intermediate of TauD that exhibits an absorption band at 318 nm.2b Notably, the downshifts of the ν(FedO) modes of 1-NCS and 1-N3 relative to that of 1, which reflect the substitution of the π-acidic CH3CN with the more π-basic N3- and NCS- ligands, yield ν(FedO) frequencies closer to that observed for the TauD intermediate (821 cm-1).2b Intriguingly, no NCS-- or N3--related vibrations were observed in the RR spectra of 1-NCS and 1-N3, suggesting that the nearUV features of these two complexes do not arise from transitions involving these axial ligands but are instead O2- f FeIV charge transfer (CT) in nature. While the corresponding O2- f FeIV CT transition of parent complex 1 has not yet been identified, the lowest energy electronic absorption band for 1 that carries significant intensity ( ≈ 10 000 M-1 cm-1) is observed at 282 nm, placing a lower energy limit on the O2- f FeIV CT transition energy of this species. Thus, taken together, these data suggest that replacement of NCCH3 in 1 by NCS- or N3- dramatically lowers the energy of the O2- f FeIV CT transition, shifting it to a value just 50006000 cm-1 below that of the corresponding transition of the highspin oxoiron(IV) intermediate of TauD.2a The axial ligand effect on the reactivity of our nonheme oxoiron(IV) complexes was also investigated by carrying out the oxidation of PPh3 with 1, 1-NCS, and 1-N3. Upon addition of PPh3 to solutions containing the nonheme oxoiron(IV) species, these intermediates reverted back to the starting iron(II) complexes, yielding Ph3PO quantitatively. Second-order rate constants extracted from these experiments at 0 °C (Table 1; Supporting Information, Figure S5) showed a difference of as much as a factor of 30, with
reactivity decreasing in the order of 1, 1-N3, and 1-NCS. These results demonstrate that the reactivity of these nonheme oxoiron(IV) complexes can be significantly affected by the identity of the axial ligand, as observed for oxoiron(IV) porphyrin π-cation radical complexes.5,6 In conclusion, treatment of 2-NCS and 2-N3 with PhIO yields the S ) 1 FeIVdO species 1-NCS and 1-N3, respectively, which have ∆EQ parameters and electronic absorption spectra quite different from those of parent complex 1. The unique near-UV absorption features of 1-NCS and 1-N3 have allowed us to make the first observation of ν(FedO) vibrations of S ) 1 mononuclear nonheme oxoiron(IV) complexes by RR spectroscopy. Additionally, we have demonstrated that the reactivity of nonheme oxoiron(IV) intermediates is markedly influenced by the axial ligands. Given the paucity of either S ) 1 or S ) 2 nonheme oxoiron(IV) complexes, it is not well established which chemical properties are governed by the FeIV spin state. It is thus noteworthy that 1-NCS and 1-N3, which have S ) 1 FeIV centers, exhibit O2- f FeIV CT transition energies and ν(FedO) frequencies quite similar to those of the S ) 2 oxoiron(IV) intermediate of TauD. Therefore, these spectroscopic signatures, which are largely governed by the FeIVdO bonding interactions, may be more sensitive to the ligand environment than the FeIV spin state, in agreement with a theoretically based proposal that FeIVdO bonding is largely unaffected by changes in spin state.9 Acknowledgment. This research was supported by the KOSEF through CRI Program (to W.N.), the U.S. NIH (GM-33162 to L.Q. and EB001475 to E.M.), Grant-in-Aid from the Ministry of Education, Culture, Sports, Science and Technology, Japan (14001004 to T.K.), and a JSPS Research Fellowship (to T.O.). Dr. Jan-Uwe Rohde is acknowledged for valuable discussions. Supporting Information Available: Text containing experimental details and Figures S1-S5. This material is available free of charge via the Internet at http://pubs.acs.org. References (1) (a) Costas, M.; Mehn, M. P.; Jensen, M. P.; Que, L., Jr. Chem. ReV. 2004, 104, 939-986. (b) Decker, A.; Solomon, E. I. Curr. Opin. Chem. Biol. 2005, 9, 152-163. (2) (a) Price, J. C.; Barr, E. W.; Tirupati, B.; Bollinger, J. M., Jr.; Krebs, C. Biochemistry 2003, 42, 7497-7508. (b) Proshlyakov, D. A.; Henshaw, T. F.; Monterosso, G. R.; Ryle, M. J.; Hausinger, R. P. J. Am. Chem. Soc. 2004, 126, 1022-1023. (c) Riggs-Gelasco, P. J.; Price, J. C.; Guyer, R. B.; Brehm, J. H.; Barr, E. W.; Bollinger, J. M., Jr.; Krebs, C. J. Am. Chem. Soc. 2004, 126, 8108-8109. (3) (a) Rohde, J.-U.; In, J.-H.; Lim, M. H.; Brennessel, W. W.; Bukowski, M. R.; Stubna, A.; Mu¨nck, E.; Nam, W.; Que, L., Jr. Science 2003, 299, 1037-1039. (b) Lim, M. H.; Rohde, J.-U.; Stubna, A.; Bukowski, M. R.; Costas, M.; Ho, R. Y. N.; Mu¨nck, E.; Nam, W.; Que, L., Jr. Proc. Natl. Acad. Sci. U.S.A. 2003, 100, 3665-3670. (c) Kaizer, J.; Klinker, E. J.; Oh, N. Y.; Rohde, J.-U.; Song, W. J.; Stubna, A.; Kim, J.; Mu¨nck, E.; Nam, W.; Que, L., Jr. J. Am. Chem. Soc. 2004, 126, 472-473. (d) Rohde, J.-U.; Torelli, S.; Shan, X.; Lim, M. H.; Klinker, E. J.; Kaizer, J.; Chen, K.; Nam, W.; Que, L., Jr. J. Am. Chem. Soc. 2004, 126, 16750-16761. (e) Kim, S. O.; Sastri, C. V.; Seo, M. S.; Kim, J.; Nam, W. J. Am. Chem. Soc. 2005, 127, 4178-4179. (4) (a) Ortiz de Montellano, P. R. Cytochrome P450: Structure, Mechanism, and Biochemistry, 3rd ed.; Kluwer Academic/Plenum Publishers: New York, 2005. (b) Denisov, I. G.; Makris, T. M.; Sligar, S. G.; Schlichting, I. Chem. ReV. 2005, 105, 2253-2277. (5) (a) Gross, Z.; Nimri, S. Inorg. Chem. 1994, 33, 1731-1732. (b) Czarnecki, K.; Nimri, S.; Gross, Z.; Proniewicz, L. M.; Kincaid, J. R. J. Am. Chem. Soc. 1996, 118, 2929-2935. (c) Fujii, H.; Yoshimura, T.; Kamada, H. Inorg. Chem. 1997, 36, 6142-6143. (6) Song, W. J.; Ryu, Y. O.; Song, R.; Nam, W. J. Biol. Inorg. Chem. 2005, 10, 294-304 and references therein. (7) See Supporting Information for the synthesis of [Fe(TMC)(X)(CF3SO3)] (X- ) NCS- and N3-) (Experimental Section), a crystal structure of [Fe(TMC)(NCS)]+ (Figure S1), and ESI MS of the iron complexes (Figure S2). (8) Rohde, J.-U.; Que, L., Jr. Angew. Chem., Int. Ed. 2005, 44, 2255-2258. (9) Decker, A.; Rohde, J.-U.; Que, L., Jr.; Solomon, E. I. J. Am. Chem. Soc. 2004, 126, 5378-5379.
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